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Comparative morphology refines the conventional model of spider reproduction.

ABSTRACT: Our understanding of spider reproductive biology is hampered by the vast anatomical diversity and difficulties associated with its study. Although authors agree on the two general types of female spider genitalia, haplogyne (plesiomorphic) and entelegyne (apomorphic), our understanding of variation within each group mostly concerns the external genital part, while the internal connections with the reproductive duct are largely unknown. Conventionally and simplistically, the spermathecae of haplogynes have simple two-way ducts, and those of entelegynes have separate copulatory and fertilization ducts for sperm to be transferred in and out of spermathecae, respectively. Sperm is discharged from the spermathecae directly into the uterus externus (a distal extension of the oviduct), which, commonly thought as homologous in both groups, is the purported location of internal fertilization in spiders. However, the structural evolution from haplo- to entelegyny remains unresolved, and thus the precise fertilization site in entelegynes is ambiguous. We aim to clarify this anatomical problem through a widely comparative morphological study of internal female genital system in entelegynes. Our survey of 147 epigyna (121 examined species in 97 genera, 34 families) surprisingly finds no direct connection between the fertilization ducts and the uterus externus, which, based on the homology with basal-most spider lineages, is a dead-end caecum in entelegynes. Instead, fertilization ducts usually connect with a secondary uterus externus, a novel feature taking over the functional role of the plesiomorphic uterus externus. We hypothesize that the transition from haplo- to entelegyny entailed not only the emergence of the two separate duct systems (copulatory, fertilization), but also involved substantial morphological changes in the distal part of the oviduct. Thus, the common oviduct may have shifted its distal connection from the uterus externus to the secondary uterus externus, perhaps facilitating discharge of larger eggs. Our findings suggest that the conventional model of entelegyne reproduction needs redefinition.

SUBMITTER: Zhan Y

PROVIDER: S-EPMC6611574 | biostudies-other | 2019

REPOSITORIES: biostudies-other

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Comparative morphology refines the conventional model of spider reproduction.

Zhan Yongjia Y Jiang He H Wu Qingqing Q Zhang Huitao H Bai Zishang Z Kuntner Matjaž M Tu Lihong L

PloS one 20190705 7

Our understanding of spider reproductive biology is hampered by the vast anatomical diversity and difficulties associated with its study. Although authors agree on the two general types of female spider genitalia, haplogyne (plesiomorphic) and entelegyne (apomorphic), our understanding of variation within each group mostly concerns the external genital part, while the internal connections with the reproductive duct are largely unknown. Conventionally and simplistically, the spermathecae of haplo ...[more]

PMID: 31276510

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Project description:BackgroundMating generally occurs after individuals reach adulthood. In many arthropods including spiders, the adult stage is marked by a final moult after which the genitalia are fully developed and functional. In several widow spider species (genus Latrodectus), however, immature females may mate a few days before they moult to adulthood, i.e. in their late-subadult stage. While the "adult" mating typically results in cannibalism, males survive the "immature" mating. During both "immature" and "adult" matings, males leave parts of their paired copulatory organs within female genitalia, which may act as mating plugs. To study potential costs and benefits of the two mating tactics, we investigated female genital morphology of the brown widow spider, L. geometricus. Light microscopy, histology and micro-computed tomography of early-subadult, late-subadult and adult females were conducted to determine the overall pattern of genital maturation. We compared genitalia of mated late-subadult and adult females to reveal potential differences in the genitalic details that might indicate differential success in sperm transfer and different environments for sperm storage and sperm competition.ResultsWe found that the paired sperm storage organs (spermathecae) and copulatory ducts are developed already in late-subadult females and host sperm after immature mating. However, the thickness of the spermathecal cuticle and the staining of the secretions inside differ significantly between the late-subadult and adult females. In late-subadult females mating plugs were found with higher probability in both spermathecae compared to adult females.ConclusionsSperm transfer in matings with late-subadult females follows the same route as in matings with adult females. The observed differences in the secretions inside the spermathecae of adult and late-subadult females likely reflect different storage conditions for the transferred sperm which may lead to a disadvantage under sperm competition if the subadult female later re-mates with another male. However, since males mating with late-subadult females typically transfer sperm to both spermathecae they might benefit from numerical sperm competition as well as from monopolizing access to the female sperm storage organs. The assessment of re-mating probability and relative paternity will clarify the costs and benefits of the two mating tactics in light of these findings.

Project description:The island nation of Madagascar is home to three endemic species of Old World fruit bat in the family Pteropodidae: Pteropus rufus, Eidolon dupreanum, and Rousettus madagascariensis, all three of which are IUCN Red Listed under some category of threat. Delineation of seasonal limits in the reproductive calendar for threatened mammals can inform conservation efforts by clarifying parameters used in population viability models, as well as elucidate understanding of the mechanisms underpinning pathogen persistence in host populations. Here, we define the seasonal limits of a staggered annual birth pulse across the three species of endemic Madagascar fruit bat, known reservoirs for viruses of high zoonotic potential. Our field studies indicate that this annual birth pulse takes place in September/October for P. rufus, November for E. dupreanum, and December for R. madagascariensis in central-eastern Madagascar where the bulk of our research was concentrated. Juvenile development periods vary across the three Malagasy pteropodids, resulting in near-synchronous weaning of pups for all species in late January-February at the height of the fruiting season for this region. We here document the size range in morphological traits for the three Malagasy fruit bat species, with P. rufus and E. dupreanum among the larger of pteropodids globally and R. madagascariensis among the smaller. All three species demonstrate subtle sexual dimorphism with males being larger than females. We explore seasonal variation in adult body condition by comparing observed body mass with body mass predicted by forearm length, demonstrating that pregnant females add weight during staggered gestation periods and males lose weight during the nutritionally deficit Malagasy winter. Finally, we quantify forearm, tibia, and ear length growth rates in juvenile bats, demonstrating both faster growth and more protracted development times for P. rufus as compared with E. dupreanum and R. madagascariensis. The longer development period for the already-threatened P. rufus further undermines the conservation status of this species as human hunting is particularly detrimental to population viability during reproductive periods. Our work highlights the importance of longitudinal field studies in collecting critical data for mammalian conservation efforts and human public health alike.

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Comparative morphology refines the conventional model of spider reproduction.

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Comparative morphology refines the conventional model of spider reproduction.

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